1887

Abstract

The presence of Wolbachia confers virus protection to insects. The molecular mechanism underlying Wolbachia-mediated protection in this tripartite host–endosymbiont–virus interaction is not yet fully understood. In the bipartite association between Drosophila melanogaster and Drosophila C virus (DCV), changes in the expression of microRNAs (miRNAs) influence the outcome of viral pathogenesis. Here we examined whether changes in miRNA expression are similarly involved in the DrosophilaWolbachia–DCV association. The levels of highly abundant miRNAs in D. melanogaster, Wolbachia-mono-infected D. melanogaster, and DCV- and Wolbachia-bi-infected D. melanogaster were quantified using RT-qPCR and compared. The results show that the abundance of the 17 tested D. melanogaster miRNAs is not affected by Wolbachia endosymbiosis or by bi-infection of Wolbachia and DCV. These results suggest that the in vivo protection conferred by Wolbachia to its native host against D. melanogaster’s natural pathogen DCV is not likely to be dependent on or associated with changes in the levels of highly expressed miRNAs.

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2018-04-20
2019-09-18
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References

  1. Hertig M, Wolbach SB. Studies on rickettsia-like micro-organisms in insects. J Med Res 1924; 44: 329– U322 [PubMed]
    [Google Scholar]
  2. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. How many species are infected with Wolbachia? – A statistical analysis of current data. FEMS Microbiol Lett 2008; 281: 215– 220 [CrossRef] [PubMed]
    [Google Scholar]
  3. Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 2012; 7: e38544 e38544 [CrossRef] [PubMed]
    [Google Scholar]
  4. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009; 139: 1268– 1278 [CrossRef] [PubMed]
    [Google Scholar]
  5. Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One 2010; 5: e13398 8 [CrossRef] [PubMed]
    [Google Scholar]
  6. Glaser RL, Meola MA. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 2010; 5: e11977 [CrossRef] [PubMed]
    [Google Scholar]
  7. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011; 476: 450– 453 [CrossRef] [PubMed]
    [Google Scholar]
  8. Dutra HL, Rocha MN, Dias FB, Mansur SB, Caragata EP et al. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe 2016; 19: 771– 774 [CrossRef] [PubMed]
    [Google Scholar]
  9. Aliota MT, Peinado SA, Velez ID, Osorio JE. The wMel strain of Wolbachia reduces transmission of zika virus by Aedes aegypti. Sci Rep 2016; 6: 28792 [CrossRef] [PubMed]
    [Google Scholar]
  10. Aliota MT, Walker EC, Uribe Yepes A, Velez ID, Christensen BM et al. The wMel strain of Wolbachia reduces transmission of chikungunya virus in Aedes aegypti. PLoS Negl Trop Dis 2016; 10: e0004677 [CrossRef] [PubMed]
    [Google Scholar]
  11. Blagrove MS, Arias-Goeta C, Failloux AB, Sinkins SP. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc Natl Acad Sci USA 2012; 109: 255– 260 [CrossRef] [PubMed]
    [Google Scholar]
  12. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. Wolbachia and virus protection in insects. Science 2008; 322: 702 [CrossRef] [PubMed]
    [Google Scholar]
  13. Teixeira L, Ferreira A, Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 2008; 6: e1000002 [CrossRef] [PubMed]
    [Google Scholar]
  14. Osborne SE, Leong YS, O'Neill SL, Johnson KN. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 2009; 5: e1000656 [CrossRef] [PubMed]
    [Google Scholar]
  15. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 2012; 78: 6922– 6929 [CrossRef] [PubMed]
    [Google Scholar]
  16. Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 2012; 6: e1754-e1754 e1754 [CrossRef] [PubMed]
    [Google Scholar]
  17. Martinez J, Longdon B, Bauer S, Chan YS, Miller WJ et al. Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog 2014; 10: e1004369 [CrossRef] [PubMed]
    [Google Scholar]
  18. Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN et al. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog 2013; 9: e1003459 [CrossRef] [PubMed]
    [Google Scholar]
  19. Caragata E, Rancès E, O'Neill SL, McGraw EA. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol 2014; 67: 205– 218 [CrossRef] [PubMed]
    [Google Scholar]
  20. Molloy JC, Sommer U, Viant MR, Sinkins SP. Wolbachia modulates lipid metabolism in Aedes albopictus mosquito cells. Appl Environ Microbiol 2016; 82: 3109– 3120 [CrossRef] [PubMed]
    [Google Scholar]
  21. Wong ZS, Brownlie JC, Johnson KN. Oxidative stress correlates with Wolbachia-mediated antiviral protection in Wolbachia-Drosophila associations. Appl Environ Microbiol 2015; 81: 3001– 3005 [CrossRef] [PubMed]
    [Google Scholar]
  22. Mcgraw E, O'Neill S. Wolbachia pipientis: intracellular infection and pathogenesis in Drosophila. Curr Opin Microbiol 2004; 7: 67– 70 [CrossRef]
    [Google Scholar]
  23. Kambris Z, Cook PE, Phuc HK, Sinkins SP. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 2009; 326: 134– 136 [CrossRef] [PubMed]
    [Google Scholar]
  24. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC et al. Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 2010; 6: e1001143 [CrossRef] [PubMed]
    [Google Scholar]
  25. Johnson KN. The impact of Wolbachia on virus infection in mosquitoes. Viruses 2015; 7: 5705– 5717 [CrossRef] [PubMed]
    [Google Scholar]
  26. Terradas G, McGraw EA. Wolbachia-mediated virus blocking in the mosquito vector Aedes aegypti. Curr Opin Insect Sci 2017; 22: 37– 44 [CrossRef] [PubMed]
    [Google Scholar]
  27. Asgari S. Regulatory role of cellular and viral microRNAs in insect–virus interactions. Curr Opin Insect Sci 2015; 8: 104– 110 [CrossRef]
    [Google Scholar]
  28. Monsanto-Hearne V, Asad S, Asgari S, Johnson KN. Drosophila microRNA modulates viral replication by targeting a homologue of mammalian cJun. J Gen Virol 2017; 98: 1904– 1912 [CrossRef] [PubMed]
    [Google Scholar]
  29. Bartel D. MicroRNA: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281– 297 [Crossref]
    [Google Scholar]
  30. Grassmann R, Jeang K-T. The roles of microRNAs in mammalian virus infection. Biochim Biophys Acta 1779; 2008: 706– 711
    [Google Scholar]
  31. Cullen BR. Viruses and microRNAs. Nat Genet 2006; 38: S25– S30 [CrossRef] [PubMed]
    [Google Scholar]
  32. Gottwein E, Cullen BR. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 2008; 3: 375– 387 [CrossRef]
    [Google Scholar]
  33. Friedman RC, Farh KK-H, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19: 92– 105 [CrossRef]
    [Google Scholar]
  34. Cullen BR. Viruses and microRNAs: RISCy interactions with serious consequences. Genes Dev 2011; 25: 1881– 1894 [CrossRef]
    [Google Scholar]
  35. Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 2015; 16: 421– 433 [CrossRef]
    [Google Scholar]
  36. Vidigal JA, Ventura A. The Biological Functions of Mirnas: Lessons from in Vivo Studies 2015; pp. 137– 147
    [Google Scholar]
  37. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014; 15: 509– 524 [CrossRef]
    [Google Scholar]
  38. Cai Y, Yu X, Hu S, Yu J. A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics 2009; 7: 147– 154 [CrossRef] [PubMed]
    [Google Scholar]
  39. Asgari S. Role of microRNAs in Insect host-microorganism interactions. Front Physiol 2011; 2: 48 [CrossRef] [PubMed]
    [Google Scholar]
  40. Gulyaeva LF, Kushlinskiy NE. Regulatory mechanisms of microRNA expression. J Transl Med 2016; 14: [CrossRef]
    [Google Scholar]
  41. Monsanto-Hearne V, Tham ALY, Wong ZS, Asgari S, Johnson KN. Drosophila miR-956 suppression modulates Ectoderm-expressed 4 and inhibits viral replication. Virology 2017; 502: 20– 27 [CrossRef]
    [Google Scholar]
  42. Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci U S A 2011; 108: 9250– 9255 [CrossRef]
    [Google Scholar]
  43. Zhang G, Hussain M, O'Neill SL, Asgari S. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc Natl Acad Sci U S A 2013; 110: 10276– 10281 [CrossRef]
    [Google Scholar]
  44. Rainey SM, Martinez J, McFarlane M, Juneja P, Sarkies P et al. Wolbachia blocks viral genome replication early in infection without a transcriptional response by the endosymbiont or host small RNA pathways. PLoS Pathog 2016; 12: e1005536 [CrossRef]
    [Google Scholar]
  45. Chrostek E, Marialva MSP, Yamada R, O'Neill SL, Teixeira L. High anti-viral protection without immune upregulation after interspecies Wolbachia transfer. PLoS One 2014; 9: e99025 [CrossRef]
    [Google Scholar]
  46. Stevanovic AL, Arnold PA, Johnson KN. Wolbachia-mediated antiviral protection in Drosophila larvae and adults following oral infection. Appl Environ Microbiol 2015; 81: 8215– 8223 [CrossRef]
    [Google Scholar]
  47. Johnson KN, Christian PD. Molecular characterization of Drosophila C virus isolates. J Invertebr Pathol 1999; 73: 248– 254 [CrossRef]
    [Google Scholar]
  48. Hedges LM, Johnson KN. Induction of host defence responses by Drosophila C virus. J Gen Virol 2008; 89: 1497– 1501 [CrossRef]
    [Google Scholar]
  49. Thomas S, Verma J, Woolfit M, O’Neill SL, Neill SL. Wolbachia-mediated virus blocking in mosquito cells is dependent on XRN1-mediated viral RNA degradation and influenced by viral replication rate. PLoS Pathog 2018; 14: e1006879 [CrossRef]
    [Google Scholar]
  50. Rancès E, Ye YH, Woolfit M, McGraw EA, O'Neill SL. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 2012; 8: e1002548 e1002548 [CrossRef]
    [Google Scholar]
  51. Saucereau Y, Valiente Moro C, Dieryckx C, Dupuy J-W, Tran F-H et al. Comprehensive proteome profiling in Aedes albopictus to decipher Wolbachia-arbovirus interference phenomenon. BMC Genomics 2017; 18: 635 [CrossRef]
    [Google Scholar]
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